In electroreceptive jawed vertebrates, embryonic lateral line placodes give rise to electrosensory ampullary organs as well as mechanosensory neuromasts. Previous reports of shared gene expression suggest that conserved mechanisms underlie electroreceptor and mechanosensory hair cell development and that electroreceptors evolved as a transcriptionally related "sister cell type" to hair cells. We previously identified only one transcription factor gene, Neurod4, as ampullary organ-restricted in the developing lateral line system of a chondrostean ray-finned fish, the Mississippi paddlefish (Polyodon spathula). The other 16 transcription factor genes we previously validated in paddlefish were expressed in both ampullary organs and neuromasts. Here, we used our published lateral line organ-enriched gene-set (arising from differential bulk RNA-seq in late-larval paddlefish), together with a candidate gene approach, to identify 25 transcription factor genes expressed in the developing lateral line system of a more experimentally tractable chondrostean, the sterlet (Acipenser ruthenus, a small sturgeon), and/or that of paddlefish. Thirteen are expressed in both ampullary organs and neuromasts, consistent with conservation of molecular mechanisms. Seven are electrosensory-restricted on the head (Irx5, Irx3, Insm1, Sp5, Satb2, Mafa and Rorc), and five are the first-reported mechanosensory-restricted transcription factor genes (Foxg1, Sox8, Isl1, Hmx2 and Rorb). However, as previously reported, Sox8 is expressed in ampullary organs as well as neuromasts in a catshark (Scyliorhinus canicula), suggesting the existence of lineage-specific differences between cartilaginous and ray-finned fishes. Overall, our results support the hypothesis that ampullary organs and neuromasts develop via largely conserved transcriptional mechanisms, and identify multiple transcription factors potentially involved in the formation of electrosensory versus mechanosensory lateral line organs.

Department of Genetics University of Cambridge Cambridge United Kingdom

Department of Physiology Development and Neuroscience University of Cambridge Cambridge United Kingdom

Department of Zoology University of Cambridge Cambridge United Kingdom

Faculty of Fisheries and Protection of Waters Research Institute of Fish Culture and Hydrobiology University of South Bohemia in České Budějovice Vodňany Czechia

Josephine Bay Paul Center for Comparative Molecular Biology and Evolution Marine Biological Laboratory Woods Hole MA United States

Zobrazit více v PubMed

Ahmed M., Wong E. Y. M., Sun J., Xu J., Wang F., Xu P.-X. (2012). Eya1-Six1 interaction is sufficient to induce hair cell fate in the cochlea by activating Atoh1 expression in cooperation with Sox2. Dev. Cell 22, 377–390. 10.1016/j.devcel.2011.12.006 PubMed DOI PMC

Baek S., Tran N. T. T., Diaz D. C., Tsai Y.-Y., Acedo J. N., Lush M. E., et al. (2022). Single-cell transcriptome analysis reveals three sequential phases of gene expression during zebrafish sensory hair cell regeneration. Dev. Cell 57, 799–819. 10.1016/j.devcel.2022.03.001 PubMed DOI PMC

Baker C. V. H. (2019). “The development and evolution of lateral line electroreceptors: insights from comparative molecular approaches,” in Electroreception: Fundamental Insights from Comparative Approaches. Editors Carlson B. A., Sisneros J. A., Popper A. N., Fay R. R. (Cham: Springer; ), 25–62. Available at: https://link.springer.com/chapter/10.1007/978-3-030-29105-1_2 . DOI

Baker C. V. H., Modrell M. S. (2018). Insights into electroreceptor development and evolution from molecular comparisons with hair cells. Integr. Comp. Biol. 58, 329–340. 10.1093/icb/icy037 PubMed DOI PMC

Baker C. V. H., Modrell M. S., Gillis J. A. (2013). The evolution and development of vertebrate lateral line electroreceptors. J. Exp. Biol. 216, 2515–2522. 10.1242/jeb.082362 PubMed DOI PMC

Ballard W. W., Mellinger J., Lechenault H. (1993). A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scylorhinidae). J. Exp. Zool. 267, 318–336. 10.1002/jez.1402670309 DOI

Baloch A. R., Franěk R., Tichopád T., Fučíková M., Rodina M., Pšenička M. (2019). Dnd1 knockout in sturgeons by CRISPR/Cas9 generates germ cell free host for surrogate production. Animals 9, 174. 10.3390/ani9040174 PubMed DOI PMC

Bardot E. S., Valdes V. J., Zhang J., Perdigoto C. N., Nicolis S., Hearn S. A., et al. (2013). Polycomb subunits Ezh1 and Ezh2 regulate the Merkel cell differentiation program in skin stem cells. EMBO J. 32, 1990–2000. 10.1038/emboj.2013.110 PubMed DOI PMC

Bellono N. W., Leitch D. B., Julius D. (2017). Molecular basis of ancestral vertebrate electroreception. Nature 543, 391–396. 10.1038/nature21401 PubMed DOI PMC

Bellono N. W., Leitch D. B., Julius D. (2018). Molecular tuning of electroreception in sharks and skates. Nature 558, 122–126. 10.1038/s41586-018-0160-9 PubMed DOI PMC

Bemis W. E., Grande L. (1992). Early development of the actinopterygian head. I. External development and staging of the paddlefish Polyodon spathula . J. Morphol. 213, 47–83. 10.1002/jmor.1052130106 PubMed DOI

Bennett M. V. L., Obara S. (1986). “Ionic mechanisms and pharmacology of electroreceptors,” in Electroreception. Editors Bullock T. H., Heiligenberg W. (New York: Wiley; ), 157–181.

Bertrand S., Thisse B., Tavares R., Sachs L., Chaumot A., Bardet P. L., et al. (2007). Unexpected novel relational links uncovered by extensive developmental profiling of nuclear receptor expression. PLoS Genet. 3, e188. 10.1371/journal.pgen.0030188 PubMed DOI PMC

Bodznick D., Montgomery J. C. (2005). “The physiology of low-frequency electrosensory systems,” in Electroreception. Editors Bullock T. H., Hopkins C. D., Popper A. N., Fay R. R. (New York: Springer; ), 132–153. Available at: https://link.springer.com/chapter/10.1007/0-387-28275-0_6 . DOI

Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Bonilla-Claudio M., Wang J., Bai Y., Klysik E., Selever J., Martin J. F. (2012). Bmp signaling regulates a dose-dependent transcriptional program to control facial skeletal development. Development 139, 709–719. 10.1242/dev.073197 PubMed DOI PMC

Bosse A., Stoykova A., Nieselt-Struwe K., Chowdhury K., Copeland N. G., Jenkins N. A., et al. (2000). Identification of a novel mouse Iroquois homeobox gene, Irx5, and chromosomal localisation of all members of the mouse Iroquois gene family. Dev. Dyn. 218, 160–174. 10.1002/(SICI)1097-0177(200005)218:1<160::AID-DVDY14>3.0.CO;2-2 PubMed DOI

Brown T. L., Horton E. C., Craig E. W., Goo C. E. A., Black E. C., Hewitt M. N., et al. (2023). Dermal appendage-dependent patterning of zebrafish atoh1a+ Merkel cells. eLife 12, e85800. 10.7554/eLife.85800 PubMed DOI PMC

Butts T., Modrell M. S., Baker C. V. H., Wingate R. J. T. (2014). The evolution of the vertebrate cerebellum: absence of a proliferative external granule layer in a non-teleost ray-finned fish. Evol. Dev. 16, 92–100. 10.1111/ede.12067 PubMed DOI PMC

Buzzi A. L., Chen J., Thiery A., Delile J., Streit A. (2022). Sox8 remodels the cranial ectoderm to generate the ear. Proc. Natl. Acad. Sci. U.S.A. 119, e2118938119. 10.1073/pnas.2118938119 PubMed DOI PMC

Camacho S., Ostos M. D. V., Llorente J. I., Sanz A., García M., Domezain A., et al. (2007). Structural characteristics and development of ampullary organs in Acipenser naccarii . Anat. Rec. 290, 1178–1189. 10.1002/ar.20569 PubMed DOI

Capella-Gutiérrez S., Silla-Martínez J. M., Gabaldón T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973. 10.1093/bioinformatics/btp348 PubMed DOI PMC

Caprara G. A., Peng A. W. (2022). Mechanotransduction in mammalian sensory hair cells. Mol. Cell. Neurosci. 120, 103706. 10.1016/j.mcn.2022.103706 PubMed DOI PMC

Cardeña-Núñez S., Sánchez-Guardado L. Ó., Corral-San-Miguel R., Rodríguez-Gallardo L., Marín F., Puelles L., et al. (2016). Expression patterns of Irx genes in the developing chick inner ear. Brain Struct. Funct. 222, 2071–2092. 10.1007/s00429-016-1326-6 PubMed DOI

Chagnaud B. P., Wilkens L. A., Hofmann M. (2021). “The ampullary electrosensory system—a paddlefish case study,” in The Senses: A Comprehensive Reference. Editor Fritzsch B. (Elsevier; ), 215–227. 10.1016/B978-0-12-809324-5.24210-7 DOI

Chen J., Wang W., Tian Z., Dong Y., Dong T., Zhu H., et al. (2018). Efficient gene transfer and gene editing in sterlet (Acipenser ruthenus). Front. Genet. 9, 117. 10.3389/fgene.2018.00117 PubMed DOI PMC

Chen Y., Gu Y., Li Y., Li G. L., Chai R., Li W., et al. (2021). Generation of mature and functional hair cells by co-expression of Gfi1, Pou4f3, and Atoh1 in the postnatal mouse cochlea. Cell Rep. 35, 109016. 10.1016/j.celrep.2021.109016 PubMed DOI

Cheng C. W., Chow R. L., Lebel M., Sakuma R., Cheung H.O.-L., Thanabalasingham V., et al. (2005). The Iroquois homeobox gene, Irx5, is required for retinal cone bipolar cell development. Dev. Biol. 287, 48–60. 10.1016/j.ydbio.2005.08.029 PubMed DOI

Cheng P., Huang Y., Lv Y., Du H., Ruan Z., Li C., et al. (2021). The American paddlefish genome provides novel insights into chromosomal evolution and bone mineralization in early vertebrates. Mol. Biol. Evol. 38, 1595–1607. 10.1093/molbev/msaa326 PubMed DOI PMC

Crampton W. G. R. (2019). Electroreception, electrogenesis and electric signal evolution. J. Fish Biol. 95, 92–134. 10.1111/jfb.13922 PubMed DOI

Dabdoub A., Puligilla C., Jones J. M., Fritzsch B., Cheah K. S., Pevny L. H., et al. (2008). Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc. Natl. Acad. Sci. U.S.A. 105, 18396–18401. 10.1073/pnas.0808175105 PubMed DOI PMC

Deprez M., Zaragosi L. E., Truchi M., Becavin C., Ruiz García S., Arguel M. J., et al. (2020). A single-cell atlas of the human healthy airways. Am. J. Respir. Crit. Care Med. 202, 1636–1645. 10.1164/rccm.201911-2199OC PubMed DOI

Dettlaff T. A., Ginsburg A. S., Schmalhausen O. I. (1993). Sturgeon Fishes: Developmental Biology and Aquaculture. Berlin: Springer-Verlag. Available at: https://link.springer.com/book/10.1007/978-3-642-77057-9 . DOI

Dirksen M.-L., Jamrich M. (1995). Differential expression of fork head genes during early Xenopus and zebrafish development. Dev. Genet. 17, 107–116. 10.1002/dvg.1020170203 PubMed DOI

Du A., Hunter C. S., Murray J., Noble D., Cai C.-L., Evans S. M., et al. (2009). Islet-1 is required for the maturation, proliferation, and survival of the endocrine pancreas. Diabetes 58, 2059–2069. 10.2337/db08-0987 PubMed DOI PMC

Du K., Stöck M., Kneitz S., Klopp C., Woltering J. M., Adolfi M. C., et al. (2020). The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nat. Ecol. Evol. 4, 841–852. 10.1038/s41559-020-1166-x PubMed DOI PMC

Dufourcq P., Roussigné M., Blader P., Rosa F., Peyrieras N., Vriz S. (2006). Mechano-sensory organ regeneration in adults: the zebrafish lateral line as a model. Mol. Cell. Neurosci. 33, 180–187. 10.1016/j.mcn.2006.07.005 PubMed DOI

Duggan C. D., Demaria S., Baudhuin A., Stafford D., Ngai J. (2008). Foxg1 is required for development of the vertebrate olfactory system. J. Neurosci. 28, 5229–5239. 10.1523/JNEUROSCI.1134-08.2008 PubMed DOI PMC

Dvorakova M., Macova I., Bohuslavova R., Anderova M., Fritzsch B., Pavlinkova G. (2020). Early ear neuronal development, but not olfactory or lens development, can proceed without SOX2. Dev. Biol. 457, 43–56. 10.1016/j.ydbio.2019.09.003 PubMed DOI PMC

Dykes I. M., Tempest L., Lee S.-I., Turner E. E. (2011). Brn3a and Islet1 act epistatically to regulate the gene expression program of sensory differentiation. J. Neurosci. 31, 9789–9799. 10.1523/JNEUROSCI.0901-11.2011 PubMed DOI PMC

Eagleson G. W., Dempewolf R. D. (2002). The role of the anterior neural ridge and Fgf-8 in early forebrain patterning and regionalization in Xenopus laevis . Comp. Biochem. Physiol. B Biochem. Mol. Biol. 132, 179–189. 10.1016/s1096-4959(01)00521-8 PubMed DOI

Elliott K. L., Fritzsch B. (2021). “Evolution and development of lateral line and electroreception: an integrated perception of neurons, hair cells and brainstem nuclei,” in The Senses: A Comprehensive Reference. Editor Fritzsch B. (Elsevier; ), 95–115. 10.1016/B978-0-12-809324-5.24170-9 DOI

Elliott K. L., Fritzsch B., Duncan J. S. (2018). Evolutionary and developmental biology provide insights into the regeneration of organ of Corti hair cells. Front. Cell. Neurosci. 12, 252. 10.3389/fncel.2018.00252 PubMed DOI PMC

England S. J., Cerda G. A., Kowalchuk A., Sorice T., Grieb G., Lewis K. E. (2020). Hmx3a has essential functions in zebrafish spinal cord, ear and lateral line development. Genetics 216, 1153–1185. 10.1534/genetics.120.303748 PubMed DOI PMC

Fauber B. P., Magnuson S. (2014). Modulators of the nuclear receptor retinoic acid receptor-related orphan receptor-γ (RORγ or RORc). J. Med. Chem. 57, 5871–5892. 10.1021/jm401901d PubMed DOI

Feng Y., Xu Q. (2010). Pivotal role of hmx2 and hmx3 in zebrafish inner ear and lateral line development. Dev. Biol. 339, 507–518. 10.1016/j.ydbio.2009.12.028 PubMed DOI

Filova I., Pysanenko K., Tavakoli M., Vochyanova S., Dvorakova M., Bohuslavova R., et al. (2022). ISL1 is necessary for auditory neuron development and contributes toward tonotopic organization. Proc. Natl. Acad. Sci. U.S.A. 119, e2207433119. 10.1073/pnas.2207433119 PubMed DOI PMC

Freitas R., Zhang G., Albert J. S., Evans D. H., Cohn M. J. (2006). Developmental origin of shark electrosensory organs. Evol. Dev. 8, 74–80. 10.1111/j.1525-142X.2006.05076.x PubMed DOI

Gibbs M. A., Northcutt R. G. (2004a). Development of the lateral line system in the shovelnose sturgeon. Brain Behav. Evol. 64, 70–84. 10.1159/000079117 PubMed DOI

Gibbs M. A., Northcutt R. G. (2004b). Retinoic acid repatterns axolotl lateral line receptors. Int. J. Dev. Biol. 48, 63–66. 10.1387/ijdb.15005576 PubMed DOI

Gillis J. A., Modrell M. S., Northcutt R. G., Catania K. C., Luer C. A., Baker C. V. H. (2012). Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes. Development 139, 3142–3146. 10.1242/dev.084046 PubMed DOI PMC

Gnedeva K., Hudspeth A. J. (2015). SoxC transcription factors are essential for the development of the inner ear. Proc. Natl. Acad. Sci. U.S.A. 112, 14066–14071. 10.1073/pnas.1517371112 PubMed DOI PMC

Gómez-Skarmeta J. L., Modolell J. (2002). Iroquois genes: genomic organization and function in vertebrate neural development. Curr. Opin. Genet. Dev. 12, 403–408. 10.1016/s0959-437x(02)00317-9 PubMed DOI

Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652. 10.1038/nbt.1883 PubMed DOI PMC

Grant K. A., Raible D. W., Piotrowski T. (2005). Regulation of latent sensory hair cell precursors by glia in the zebrafish lateral line. Neuron 45, 69–80. 10.1016/j.neuron.2004.12.020 PubMed DOI

Haber A. L., Biton M., Rogel N., Herbst R. H., Shekhar K., Smillie C., et al. (2017). A single-cell survey of the small intestinal epithelium. Nature 551, 333–339. 10.1038/nature24489 PubMed DOI PMC

He Y., Lu X., Qian F., Liu D., Chai R., Li H. (2017). Insm1a is required for zebrafish posterior lateral line development. Front. Mol. Neurosci. 10, 241. 10.3389/fnmol.2017.00241 PubMed DOI PMC

Hesse K., Vaupel K., Kurt S., Buettner R., Kirfel J., Moser M. (2011). AP-2δ is a crucial transcriptional regulator of the posterior midbrain. PLoS ONE 6, e23483. 10.1371/journal.pone.0023483 PubMed DOI PMC

Hoffman B. U., Baba Y., Griffith T. N., Mosharov E. V., Woo S. H., Roybal D. D., et al. (2018). Merkel cells activate sensory neural pathways through adrenergic synapses. Neuron 100, 1401–1413. 10.1016/j.neuron.2018.10.034 PubMed DOI PMC

Houweling A. C., Dildrop R., Peters T., Mummenhoff J., Moorman A. F. M., Rüther U., et al. (2001). Gene and cluster-specific expression of the Iroquois family members during mouse development. Mech. Dev. 107, 169–174. 10.1016/s0925-4773(01)00451-8 PubMed DOI

Hu X., Wang Y., Hao L.-Y., Liu X., Lesch C. A., Sanchez B. M., et al. (2015). Sterol metabolism controls TH17 differentiation by generating endogenous RORγ agonists. Nat. Chem. Biol. 11, 141–147. 10.1038/nchembio.1714 PubMed DOI

Huang M., Sage C., Li H., Xiang M., Heller S., Chen Z.-Y. (2008). Diverse expression patterns of LIM-homeodomain transcription factors (LIM-HDs) in mammalian inner ear development. Dev. Dyn. 237, 3305–3312. 10.1002/dvdy.21735 PubMed DOI PMC

Huang X., Chen Q., Luo W., Pakvasa M., Zhang Y., Zheng L., et al. (2022). SATB2: a versatile transcriptional regulator of craniofacial and skeleton development, neurogenesis and tumorigenesis, and its applications in regenerative medicine. Genes Dis. 9, 95–107. 10.1016/j.gendis.2020.10.003 PubMed DOI PMC

Hwang C. H., Simeone A., Lai E., Wu D. K. (2009). Foxg1 is required for proper separation and formation of sensory cristae during inner ear development. Dev. Dyn. 238, 2725–2734. 10.1002/dvdy.22111 PubMed DOI

Jan T. A., Eltawil Y., Ling A. H., Chen L., Ellwanger D. C., Heller S., et al. (2021). Spatiotemporal dynamics of inner ear sensory and non-sensory cells revealed by single-cell transcriptomics. Cell Rep. 36, 109358. 10.1016/j.celrep.2021.109358 PubMed DOI PMC

Jen H.-I., Singh S., Tao L., Maunsell H. R., Segil N., Groves A. K. (2022). GFI1 regulates hair cell differentiation by acting as an off-DNA transcriptional co-activator of ATOH1, and a DNA-binding repressor. Sci. Rep. 12, 7793. 10.1038/s41598-022-11931-0 PubMed DOI PMC

Jessen K. R., Mirsky R. (2019). Schwann cell precursors; multipotent glial cells in embryonic nerves. Front. Mol. Neurosci. 12, 69. 10.3389/fnmol.2019.00069 PubMed DOI PMC

Jørgensen J. M. (2005). “Morphology of electroreceptive sensory organs,” in Electroreception. Editors Bullock T. H., Hopkins C. D., Popper A. N., Fay R. R. (New York: Springer; ), 47–67. Available at: https://link.springer.com/chapter/10.1007/0-387-28275-0_3 . DOI

Kalyaanamoorthy S., Minh B. Q., Wong T. K. F., von Haeseler A., Jermiin L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589. 10.1038/nmeth.4285 PubMed DOI PMC

Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. 10.1093/molbev/mst010 PubMed DOI PMC

Kawauchi S., Santos R., Kim J., Hollenbeck P. L. W., Murray R. C., Calof A. L. (2009). The role of Foxg1 in the development of neural stem cells of the olfactory epithelium. Ann. N. Y. Acad. Sci. 1170, 21–27. 10.1111/j.1749-6632.2009.04372.x PubMed DOI PMC

Kelsh R. N., Eisen J. S. (2000). The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development 127, 515–525. 10.1242/dev.127.3.515 PubMed DOI

Kennedy M. W., Chalamalasetty R. B., Thomas S., Garriock R. J., Jailwala P., Yamaguchi T. P. (2016). Sp5 and Sp8 recruit β-catenin and Tcf1-Lef1 to select enhancers to activate Wnt target gene transcription. Proc. Natl. Acad. Sci. U.S.A. 113, 3545–3550. 10.1073/pnas.1519994113 PubMed DOI PMC

Kiernan A. E., Pelling A. L., Leung K. K., Tang A. S., Bell D. M., Tease C., et al. (2005). Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434, 1031–1035. 10.1038/nature03487 PubMed DOI

Kotas M. E., O’Leary C. E., Locksley R. M. (2023). Tuft cells: context- and tissue-specific programming for a conserved cell lineage. Annu. Rev. Pathol. 18, 311–335. 10.1146/annurev-pathol-042320-112212 PubMed DOI PMC

Koth M. L., Garcia-Moreno S. A., Novak A., Holthusen K. A., Kothandapani A., Jiang K., et al. (2020). Canonical Wnt/β-catenin activity and differential epigenetic marks direct sexually dimorphic regulation of Irx3 and Irx5 in developing mouse gonads. Development 147, dev183814. 10.1242/dev.183814 PubMed DOI PMC

Kotkamp K., Mössner R., Allen A., Onichtchouk D., Driever W. (2014). A Pou5f1/Oct4 dependent Klf2a, Klf2b, and Klf17 regulatory sub-network contributes to EVL and ectoderm development during zebrafish embryogenesis. Dev. Biol. 385, 433–447. 10.1016/j.ydbio.2013.10.025 PubMed DOI

Ladurner A., Schwarz P. F., Dirsch V. M. (2021). Natural products as modulators of retinoic acid receptor-related orphan receptors (RORs). Nat. Prod. Rep. 38, 757–781. 10.1039/d0np00047g PubMed DOI

Lecaudey V., Anselme I., Dildrop R., Rüther U., Schneider-Maunoury S. (2005). Expression of the zebrafish Iroquois genes during early nervous system formation and patterning. J. Comp. Neurol. 492, 289–302. 10.1002/cne.20765 PubMed DOI

Leitch D. B., Julius D. (2019). “Electrosensory transduction: comparisons across structure, afferent response properties, and cellular physiology,” in Electroreception: Fundamental Insights from Comparative Approaches. Editors Carlson B. A., Sisneros J. A., Popper A. N., Fay R. R. (Cham: Springer; ), 63–90. Available at: https://link.springer.com/chapter/10.1007/978-3-030-29105-1_3 . DOI

Lesko M. H., Driskell R. R., Kretzschmar K., Goldie S. J., Watt F. M. (2013). Sox2 modulates the function of two distinct cell lineages in mouse skin. Dev. Biol. 382, 15–26. 10.1016/j.ydbio.2013.08.004 PubMed DOI PMC

Li X., Gaillard F., Monckton E. A., Glubrecht D. D., Persad A. R., Moser M., et al. (2016). Loss of AP-2delta reduces retinal ganglion cell numbers and axonal projections to the superior colliculus. Mol. Brain 9, 62. 10.1186/s13041-016-0244-0 PubMed DOI PMC

Liang J., Chirikjian M., Pajvani U. B., Bartolomé A. (2022). MafA regulation in β-cells: from transcriptional to post-translational mechanisms. Biomolecules 12, 535. 10.3390/biom12040535 PubMed DOI PMC

López-Schier H., Hudspeth A. J. (2005). Supernumerary neuromasts in the posterior lateral line of zebrafish lacking peripheral glia. Proc. Natl. Acad. Sci. U.S.A. 102, 1496–1501. 10.1073/pnas.0409361102 PubMed DOI PMC

Lorenzen S. M., Duggan A., Osipovich A. B., Magnuson M. A., García-Añoveros J. (2015). Insm1 promotes neurogenic proliferation in delaminated otic progenitors. Mech. Dev. 138 Pt 3, 233–245. 10.1016/j.mod.2015.11.001 PubMed DOI PMC

Lu X., Sipe C. W. (2016). Developmental regulation of planar cell polarity and hair-bundle morphogenesis in auditory hair cells: lessons from human and mouse genetics. WIREs Dev. Biol. 5, 85–101. 10.1002/wdev.202 PubMed DOI PMC

Lush M. E., Diaz D. C., Koenecke N., Baek S., Boldt H., St Peter M. K., et al. (2019). scRNA-Seq reveals distinct stem cell populations that drive hair cell regeneration after loss of Fgf and Notch signaling. eLife 8, e44431. 10.7554/eLife.44431 PubMed DOI PMC

Mak A. C. Y., Szeto I. Y. Y., Fritzsch B., Cheah K. S. E. (2009). Differential and overlapping expression pattern of SOX2 and SOX9 in inner ear development. Gene Expr. Patterns 9, 444–453. 10.1016/j.gep.2009.04.003 PubMed DOI PMC

Martik M. L., Gandhi S., Uy B. R., Gillis J. A., Green S. A., Simoes-Costa M., et al. (2019). Evolution of the new head by gradual acquisition of neural crest regulatory circuits. Nature 574, 675–678. 10.1038/s41586-019-1691-4 PubMed DOI PMC

Matern M. S., Milon B., Lipford E. L., McMurray M., Ogawa Y., Tkaczuk A., et al. (2020). GFI1 functions to repress neuronal gene expression in the developing inner ear hair cells. Development 147, dev186015. 10.1242/dev.186015 PubMed DOI PMC

McGinnis S., Madden T. L. (2004). BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 32, W20–W25. 10.1093/nar/gkh435 PubMed DOI PMC

McGovern M. M., Hosamani I. V., Niu Y., Nguyen K. Y., Zong C., Groves A. K. (2024). Expression of Atoh1, Gfi1, and Pou4f3 in the mature cochlea reprograms nonsensory cells into hair cells. Proc. Natl. Acad. Sci. U.S.A. 121, e2304680121. 10.1073/pnas.2304680121 PubMed DOI PMC

Meijer F. A., Doveston R. G., de Vries R. M. J. M., Vos G. M., Vos A. A. A., Leysen S., et al. (2020). Ligand-based design of allosteric retinoic acid receptor-related orphan receptor γt (RORγt) inverse agonists. J. Med. Chem. 63, 241–259. 10.1021/acs.jmedchem.9b01372 PubMed DOI PMC

Metscher B. D., Müller G. B. (2011). MicroCT for molecular imaging: quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs. Dev. Dyn. 240, 2301–2308. 10.1002/dvdy.22733 PubMed DOI

Miller S. R., Perera S. N., Baker C. V. H. (2017). Constitutively active Notch1 converts cranial neural crest-derived frontonasal mesenchyme to perivascular cells in vivo . Biol. Open 6, 317–325. 10.1242/bio.023887 PubMed DOI PMC

Minh B. Q., Schmidt H. A., Chernomor O., Schrempf D., Woodhams M. D., von Haeseler A., et al. (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534. 10.1093/molbev/msaa015 PubMed DOI PMC

Modrell M. S., Baker C. V. H. (2012). Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates. Evol. Dev. 14, 277–285. 10.1111/j.1525-142X.2012.00544.x PubMed DOI PMC

Modrell M. S., Bemis W. E., Northcutt R. G., Davis M. C., Baker C. V. H. (2011a). Electrosensory ampullary organs are derived from lateral line placodes in bony fishes. Nat. Commun. 2, 496. 10.1038/ncomms1502 PubMed DOI PMC

Modrell M. S., Buckley D., Baker C. V. H. (2011b). Molecular analysis of neurogenic placode development in a basal ray-finned fish. genesis 49, 278–294. 10.1002/dvg.20707 PubMed DOI PMC

Modrell M. S., Lyne M., Carr A. R., Zakon H. H., Buckley D., Campbell A. S., et al. (2017a). Insights into electrosensory organ development, physiology and evolution from a lateral line-enriched transcriptome. eLife 6, e24197. 10.7554/eLife.24197 PubMed DOI PMC

Modrell M. S., Tidswell O. R. A., Baker C. V. H. (2017b). Notch and Fgf signaling during electrosensory versus mechanosensory lateral line organ development in a non-teleost ray-finned fish. Dev. Biol. 431, 48–58. 10.1016/j.ydbio.2017.08.017 PubMed DOI PMC

Mogdans J. (2019). Sensory ecology of the fish lateral-line system: morphological and physiological adaptations for the perception of hydrodynamic stimuli. J. Fish Biol. 95, 53–72. 10.1111/jfb.13966 PubMed DOI

Moser T., Grabner C. P., Schmitz F. (2020). Sensory processing at ribbon synapses in the retina and the cochlea. Physiol. Rev. 100, 103–144. 10.1152/physrev.00026.2018 PubMed DOI

Norris H. W., Hughes S. P. (1920). The spiracular sense-organ in elasmobranchs, ganoids and dipnoans. Anat. Rec. 18, 205–209. 10.1002/ar.1090180210 DOI

Northcutt R. G. (1997). Evolution of gnathostome lateral line ontogenies. Brain Behav. Evol. 50, 25–37. 10.1159/000113319 PubMed DOI

Northcutt R. G., Brändle K., Fritzsch B. (1995). Electroreceptors and mechanosensory lateral line organs arise from single placodes in axolotls. Dev. Biol. 168, 358–373. 10.1006/dbio.1995.1086 PubMed DOI

Northcutt R. G., Catania K. C., Criley B. B. (1994). Development of lateral line organs in the axolotl. J. Comp. Neurol. 340, 480–514. 10.1002/cne.903400404 PubMed DOI

O’Donnell M., Hong C.-S., Huang X., Delnicki R. J., Saint-Jeannet J.-P. (2006). Functional analysis of Sox8 during neural crest development in Xenopus . Development 133, 3817–3826. 10.1242/dev.02558 PubMed DOI

Ó Maoiléidigh D., Ricci A. J. (2019). A bundle of mechanisms: inner-ear hair-cell mechanotransduction. Trends Neurosci. 42, 221–236. 10.1016/j.tins.2018.12.006 PubMed DOI PMC

O’Neill P., McCole R. B., Baker C. V. H. (2007). A molecular analysis of neurogenic placode and cranial sensory ganglion development in the shark, Scyliorhinus canicula . Dev. Biol. 304, 156–181. 10.1016/j.ydbio.2006.12.029 PubMed DOI PMC

Pangrsic T., Singer J. H., Koschak A. (2018). Voltage-gated calcium channels: key players in sensory coding in the retina and the inner ear. Physiol. Rev. 98, 2063–2096. 10.1152/physrev.00030.2017 PubMed DOI PMC

Papalopulu N., Kintner C. (1996). A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122, 3409–3418. 10.1242/dev.122.11.3409 PubMed DOI

Pauley S., Lai E., Fritzsch B. (2006). Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev. Dyn. 235, 2470–2482. 10.1002/dvdy.20839 PubMed DOI PMC

Perdigoto C. N., Bardot E. S., Valdes V. J., Santoriello F. J., Ezhkova E. (2014). Embryonic maturation of epidermal Merkel cells is controlled by a redundant transcription factor network. Development 141, 4690–4696. 10.1242/dev.112169 PubMed DOI PMC

Piotrowski T., Baker C. V. H. (2014). The development of lateral line placodes: taking a broader view. Dev. Biol. 389, 68–81. 10.1016/j.ydbio.2014.02.016 PubMed DOI

Radde-Gallwitz K., Pan L., Gan L., Lin X., Segil N., Chen P. (2004). Expression of Islet1 marks the sensory and neuronal lineages in the mammalian inner ear. J. Comp. Neurol. 477, 412–421. 10.1002/cne.20257 PubMed DOI PMC

Reilly M. B., Cros C., Varol E., Yemini E., Hobert O. (2020). Unique homeobox codes delineate all the neuron classes of C. elegans . Nature 584, 595–601. 10.1038/s41586-020-2618-9 PubMed DOI PMC

Romero-Carvajal A., Navajas Acedo J., Jiang L., Kozlovskaja-Gumbriene A., Alexander R., Li H., et al. (2015). Regeneration of sensory hair cells requires localized interactions between the Notch and Wnt pathways. Dev. Cell 34, 267–282. 10.1016/j.devcel.2015.05.025 PubMed DOI PMC

Saito T., Psenicka M. (2015). Novel technique for visualizing primordial germ cells in sturgeons (Acipenser ruthenus, A. gueldenstaedtii, A. baerii, and Huso huso). Biol. Reprod. 93, 96. 10.1095/biolreprod.115.128314 PubMed DOI

Sapède D., Gompel N., Dambly-Chaudière C., Ghysen A. (2002). Cell migration in the postembryonic development of the fish lateral line. Development 129, 605–615. 10.1242/dev.129.3.605 PubMed DOI

Schulz M. H., Zerbino D. R., Vingron M., Birney E. (2012). Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28, 1086–1092. 10.1093/bioinformatics/bts094 PubMed DOI PMC

Stehlin-Gaon C., Willmann D., Zeyer D., Sanglier S., Van Dorsselaer A., Renaud J.-P., et al. (2003). All-trans retinoic acid is a ligand for the orphan nuclear receptor ROR beta. Nat. Struct. Biol. 10, 820–825. 10.1038/nsb979 PubMed DOI

Stöver B. C., Müller K. F. (2010). TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11, 7. 10.1186/1471-2105-11-7 PubMed DOI PMC

Stundl J., Pospisilova A., Matějková T., Psenicka M., Bronner M. E., Cerny R. (2020). Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes. Dev. Biol. 467, 14–29. 10.1016/j.ydbio.2020.08.007 PubMed DOI PMC

Stundl J., Soukup V., Franěk R., Pospisilova A., Psutkova V., Pšenička M., et al. (2022). Efficient CRISPR mutagenesis in sturgeon demonstrates its utility in large, slow-maturing vertebrates. Front. Cell Dev. Biol. 10, 750833. 10.3389/fcell.2022.750833 PubMed DOI PMC

Stundl J., Martik M. L., Chen D., Raja D. A., Franěk R., Pospisilova A., et al. (2023). Ancient vertebrate dermal armor evolved from trunk neural crest. Proc. Natl. Acad. Sci. U.S.A. 120, e2221120120. 10.1073/pnas.2221120120 PubMed DOI PMC

Sun Y., Dykes I. M., Liang X., Eng S. R., Evans S. M., Turner E. E. (2008). A central role for Islet1 in sensory neuron development linking sensory and spinal gene regulatory programs. Nat. Neurosci. 11, 1283–1293. 10.1038/nn.2209 PubMed DOI PMC

Sun Y., Liu Z. (2023). Recent advances in molecular studies on cochlear development and regeneration. Curr. Opin. Neurobiol. 81, 102745. 10.1016/j.conb.2023.102745 PubMed DOI

Tasdemir-Yilmaz O. E., Druckenbrod N. R., Olukoya O. O., Dong W., Yung A. R., Bastille I., et al. (2021). Diversity of developing peripheral glia revealed by single-cell RNA sequencing. Dev. Cell 56, 2516–2535.e8. 10.1016/j.devcel.2021.08.005 PubMed DOI PMC

Toresson H., Martinez-Barbera J. P., Bardsley A., Caubit X., Krauss S. (1998). Conservation of BF-1 expression in amphioxus and zebrafish suggests evolutionary ancestry of anterior cell types that contribute to the vertebrate telencephalon. Dev. Genes Evol. 208, 431–439. 10.1007/s004270050200 PubMed DOI

Undurraga C. A., Gou Y., Sandoval P. C., Nuñez V. A., Allende M. L., Riley B. B., et al. (2019). Sox2 and Sox3 are essential for development and regeneration of the zebrafish lateral line. bioRxiv 856088. 10.1101/856088 DOI

Vidal B., Gulez B., Cao W. X., Leyva-Díaz E., Reilly M. B., Tekieli T., et al. (2022). The enteric nervous system of the C. elegans pharynx is specified by the Sine oculis-like homeobox gene ceh-34 . eLife 11, e76003. 10.7554/eLife.76003 PubMed DOI PMC

votn Bartheld C. S., Giannessi F. (2011). The paratympanic organ: a barometer and altimeter in the middle ear of birds? J. Exp. Zool. B Mol. Dev. Evol. 316, 402–408. 10.1002/jez.b.21422 PubMed DOI PMC

Wang J., Lu C., Zhao Y., Tang Z., Song J., Fan C. (2020). Transcriptome profiles of sturgeon lateral line electroreceptor and mechanoreceptor during regeneration. BMC Genomics 21, 875. 10.1186/s12864-020-07293-4 PubMed DOI PMC

Wang X., Llamas J., Trecek T., Shi T., Tao L., Makmura W., et al. (2023). SoxC transcription factors shape the epigenetic landscape to establish competence for sensory differentiation in the mammalian organ of Corti. Proc. Natl. Acad. Sci. U.S.A. 120, e2301301120. 10.1073/pnas.2301301120 PubMed DOI PMC

Webb J. F. (2021). “Morphology of the mechanosensory lateral line system of fishes,” in The Senses: A Comprehensive Reference. Editor Fritzsch B. (Elsevier; ), 29–46. 10.1016/B978-0-12-809324-5.24162-X DOI

Wiwatpanit T., Lorenzen S. M., Cantú J. A., Foo C. Z., Hogan A. K., Márquez F., et al. (2018). Trans-differentiation of outer hair cells into inner hair cells in the absence of INSM1. Nature 563, 691–695. 10.1038/s41586-018-0570-8 PubMed DOI PMC

Wullimann M. F., Grothe B. (2014). “The central nervous organization of the lateral line system,” in The Lateral Line System. Editors Coombs S. C., Bleckmann H., Fay R. R., Popper A. N. (New York: Springer; ), 195–251. Available at: https://link.springer.com/chapter/10.1007/2506_2013_18 . DOI

Xu J., Li J., Zhang T., Jiang H., Ramakrishnan A., Fritzsch B., et al. (2021). Chromatin remodelers and lineage-specific factors interact to target enhancers to establish proneurosensory fate within otic ectoderm. Proc. Natl. Acad. Sci. U.S.A. 118, e2025196118. 10.1073/pnas.2025196118 PubMed DOI PMC

Yamashita T., Zheng F., Finkelstein D., Kellard Z., Robert C., Rosencrance C. D., et al. (2018). High-resolution transcriptional dissection of in vivo Atoh1-mediated hair cell conversion in mature cochleae identifies Isl1 as a co-reprogramming factor. PLoS Genet. 14, e1007552. 10.1371/journal.pgen.1007552 PubMed DOI PMC

Zeiske E., Kasumyan A., Bartsch P., Hansen A. (2003). Early development of the olfactory organ in sturgeons of the genus Acipenser: a comparative and electron microscopic study. Anat. Embryol. 206, 357–372. 10.1007/s00429-003-0309-6 PubMed DOI

Zerbino D. R., Birney E. (2008). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829. 10.1101/gr.074492.107 PubMed DOI PMC

Zhang S., Zhang Y., Dong Y., Guo L., Zhang Z., Shao B., et al. (2019). Knockdown of Foxg1 in supporting cells increases the trans-differentiation of supporting cells into hair cells in the neonatal mouse cochlea. Cell. Mol. Life Sci. 77, 1401–1419. 10.1007/s00018-019-03291-2 PubMed DOI PMC

Zhang Y., Zhang S., Zhang Z., Dong Y., Ma X., Qiang R., et al. (2020). Knockdown of Foxg1 in Sox9+ supporting cells increases the trans-differentiation of supporting cells into hair cells in the neonatal mouse utricle. Aging (Albany NY) 12, 19834–19851. 10.18632/aging.104009 PubMed DOI PMC

Zhao X.-F., Suh C. S., Prat C. R., Ellingsen S., Fjose A. (2009). Distinct expression of two foxg1 paralogues in zebrafish. Gene Expr. Patterns 9, 266–272. 10.1016/j.gep.2009.04.001 PubMed DOI

Zine A., Fritzsch B. (2023). Early steps towards hearing: placodes and sensory development. Int. J. Mol. Sci. 24, 6994. 10.3390/ijms24086994 PubMed DOI PMC